Managing Bay and Estuarine Ecosystems for …...Managing Bay and Estuarine Ecosystems for Multiple Services Lisa A. Needles & Sarah E. Lester & Richard Ambrose & Anders Andren & Marc

Managing Bay and Estuarine Ecosystems for Multiple Services

Lisa A. Needles & Sarah E. Lester & Richard Ambrose &

Anders Andren & Marc Beyeler & Michael S. Connor &

James E. Eckman & Barry A. Costa-Pierce &

Steven D. Gaines & Kevin D. Lafferty & Hunter S. Lenihan &

Julia Parrish & Mark S. Peterson & Amy E. Scaroni &Judith S. Weis & Dean E. Wendt

Received: 12 April 2012 /Revised: 28 January 2013 /Accepted: 22 February 2013# Coastal and Estuarine Research Federation 2013

Abstract Managers are moving from a model of managingindividual sectors, human activities, or ecosystem servicesto an ecosystem-based management (EBM) approach whichattempts to balance the range of services provided by eco-systems. Applying EBM is often difficult due to inherenttradeoffs in managing for different services. This challengeparticularly holds for estuarine systems, which have beenheavily altered in most regions and are often subject tointense management interventions. Estuarine managers canoften choose among a range of management tactics to

enhance a particular service; although some managementactions will result in strong tradeoffs, others may enhancemultiple services simultaneously. Management of estuarineecosystems could be improved by distinguishing betweenoptimal management actions for enhancing multiple ser-vices and those that have severe tradeoffs. This requires aframework that evaluates tradeoff scenarios and identifiesmanagement actions likely to benefit multiple services. Wecreated a management action-services matrix as a first steptowards assessing tradeoffs and providing managers with a

Electronic supplementary material The online version of this article(doi:10.1007/s12237-013-9602-7) contains supplementary material,which is available to authorized users.

L. A. Needles (*)Department of Ecology, Evolution and Marine Biologyand the Marine Science Institute, University of California,Santa Barbara, CA 93106, USAe-mail: [email protected]

D. E. WendtCenter for Coastal Marine Sciences and Department of BiologicalSciences, California Polytechnic State University,San Luis Obispo, CA 93407, USA

S. E. LesterMarine Science Institute and Bren School of EnvironmentalScience and Management, University of California,Santa Barbara, CA 93106, USA

R. AmbroseDepartment of Environmental Health Sciences, Universityof California, Los Angeles, CA 90095, USA

A. AndrenEnvironmental Chemistry and Technology Program, Universityof Wisconsin-Madison, 660 North Park Street, Madison, WI53706, USA

M. BeyelerDepartment of Sociology and Department of EnvironmentalStudies, University of California,Santa Cruz, CA 95064, USA

M. BeyelerMBA Consultants,111 El Camino Real, Berkeley, CA 94705, USA

M. S. ConnorEast Bay Dischargers Authority, 2651 Grant Ave,San Lorenzo, CA 94580, USA

J. E. EckmanCalifornia Sea Grant Program, Scripps Institution ofOceanography, University of California San Diego,La Jolla, CA 92093, USA

B. A. Costa-PierceDepartment of Marine Sciences, University of New England,11 Hills Beach Road, Biddeford, ME, USA

Estuaries and CoastsDOI 10.1007/s12237-013-9602-7

http://dx.doi.org/10.1007/s12237-013-9602-7

decision support tool. We found that management actionsthat restored or enhanced natural vegetation (e.g., salt marshand mangroves) and some shellfish (particularly oysters andoyster reef habitat) benefited multiple services. In contrast,management actions such as desalination, salt pond crea-tion, sand mining, and large container shipping had large netnegative effects on several of the other services consideredin the matrix. Our framework provides resource managers asimple way to inform EBM decisions and can also be usedas a first step in more sophisticated approaches that modelservice delivery.

Keywords Ecosystem-based management . Ecosystemservices . Estuary . Bay . Tradeoff analysis . Ecosystemfunction . Marine spatial planning . Decision support tool

Introduction

Estuaries and bays are among the most highly altered anddegraded ecosystems, yet humans depend on the health ofestuarine ecosystems for a variety of services (MEA 2005).Estuaries provide food, regulate water quality, protect againstcoastline damage and flooding by storms, provide recreationalopportunities, and aesthetic and spiritual value (Costanza et al.1997). Estuaries and bays also facilitate the transport of goodsand associated services and are emerging as an importantsource for tidal energy. In addition, estuaries serve as a nurseryhabitat for many economically important coastal species(MEA 2005; Engle 2011). Production of many of these ser-vices is declining in many estuarine systems (MEA 2005;

Lotze et al. 2006; Barbier et al. 2011); while at the same time,the demand for services provided by estuaries and bays isexpected to increase substantially (Kennish 2002).

Traditionally, management of bays and estuaries has fo-cused mostly on single sector outcomes (e.g., improved waterquality and single species recovery) and restoration of naturalecosystems to their historic composition of species. Now,ecologists and managers are increasingly focused on the res-toration of ecosystem function, rather than restoration of spe-cies per se, recognizing that some services are still providedwith a novel species composition (Lenihan and Peterson1998; Ewel and Putz 2004; Schlaepfer et al. 2011).

Shifting the management focus to the maintenance andrestoration of ecosystem function is not without its chal-lenges. First, there are different regulatory agencies andstakeholders involved in management decisions, often withcompeting mandates or objectives. For example, in theUSA, separate agencies are tasked with managing fisheries(e.g., National Oceanic and Atmospheric Administration(NOAA)), water quality (e.g., Environmental ProtectionAgency (EPA)), and energy production (e.g., Departmentof Energy). The directive of one agency (or the targets ofone stakeholder group) may be at odds with that of another.Therefore, management of estuaries is often siloed by indi-vidual sectors or services, without an explicit considerationof the functioning of the ecosystem as a whole.

The second, and potentially more problematic challenge,is that services are not independent of one another and thereare often inherent tradeoffs in implementing managementactions designed to enhance a single service (Barbier et al.2008; Bennett et al. 2009; Koch et al. 2009). Moreover,economic activities valued by society are often at odds withmaintaining or promoting ecosystem services provided byestuaries. Therefore, rather than managing for individualecosystem services or economic activities alone, managersneed to: (a) consider a suite of ecosystem services andeconomic activities in bays and estuaries and (b) predicthow they will respond to different management options.This can involve complex decisions to determine sociallydesirable outcomes given that it may not be possible tomaximize the delivery of all services (Tallis et al. 2008;Barbier 2009; Bennett et al. 2009; Nelson et al. 2009).There are also situations where services (including econom-ic activities) are either positively correlated with one anotheror show a synergistic relationship (see Bennett et al. 2009;Table 1), providing an opportunity to impart numerousbenefits. However, these types of interactions, whether pos-itive or negative, are often missing from natural resourcemanagement plans (Lenihan and Peterson 1998). This maystem in part from the tendency for management agencies tofocus on a single service but is also likely a result of thepaucity of simple and practical yet rigorous approaches forassessing service tradeoffs.

S. D. Gaines :H. S. LenihanBren School of Environmental Science and Management,University of California, Santa Barbara, CA 93106, USA

K. D. LaffertyWestern Ecological Research Center, U.S. Geological Survey,c/o Marine Science Institute, University of California,Santa Barbara, CA 93106, USA

J. ParrishSchool of Aquatic and Fishery Sciences and Biology Department,University of Washington, Seattle, WA 98195, USA

M. S. PetersonDepartment of Coastal Sciences, University of SouthernMississippi, 703 East Beach Drive, Ocean Springs, MS 39564,USA

A. E. ScaroniWye Research and Education Center, University of Maryland SeaGrant Extension, 124 Wye Narrows Drive, PO Box 169,Queenstown, MD 21658, USA

J. S. WeisDepartment of Biological Sciences, Rutgers University,Newark, NJ 07102, USA

Estuaries and Coasts

One framework for ecosystem service tradeoff analysisborrows from economic theory and multiobjective decisionmaking (White et al. 2012; Lester et al. 2013). This type ofanalysis focuses on modeling or measuring the ecosystemservice outcomes of different management approaches.

Results can then be visualized on a multidimensional graphwhere axes correspond to services of interest and each pointon the graph indicates the service outcome of a particularmanagement option (Fig. 1). The outer bound of all thepossible points is the “efficiency frontier” composed of

Table 1 Management action/service matrix

0 - -

0 - -

- +/- +/-

- -

+ - -

0 0/-

0 0 0

+/-

+ 0 0

+ +/- +

+ - -

+ - -

0/- 0 0

+/-

+ ? 0 0 0 0

?

0

0

0

0 0

- - - -

+/- + 0 0 + - 0 0/- 0 0 0 0 ?

- + +/- +/0 + - +/0 0 0 0 - 0/- -

0 0 0

+/-

+/- 0 0 0 0 0

+/- 0 0 0/- 0 0/- + - - -

+ +

+ +

+ +/- +/- + + 0 0 - 0 0 0 0/- +

0/-

MS # Service Management Action HS DV RC CY CM BP NBP PP TR FP SS NC CP BD

1Aesthetic, Historical and Spiritual Value

Viewshed protection + +/- +/- 0 +/- 0/- 0/- 0/- + + +/0


Site protection (e.g. archeological) + - +/- 0 0/- - 0/- 0/- + +/0 +/0


Species protection + - +/- 0 0 +/- 0/- 0/- 0/- +/- +/- +/- +/- +

4 Area for DevelopmentSiting, development (e.g. malls, parking lots, buildings)

- + +/- - - +/- +/- +/- 0/- - -

5 Recreation Habitat restoration/creation + - + + + + 0/- +/- + + + +

6 Recreation Habitat protection + - + + + 0/- +/- +/- + + +

7 Recreation Coastal access (e.g. trails, parking) + + + 0 +/- 0/- 0 0/- +/- 0/- - -

8 Recreation Beach nourishment +/- + + 0 - 0 0 0 0 + + - - -

9 RecreationInstallation of piers/ramps (for boating)

- + + 0/- + + 0/- +/- - - -

10 Recreation Dredging/channelization - + +/- - +/- + + + + - - - -

11 RecreationStock enhancement for recreational fisheries

+ + + 0 + 0 0 0 +/- +/- +/-

12 Climate RegulationHabitat protection - emergent vegetation (mangrove, marsh)

+ - +/- + + + - 0/- - + + + + +

13 Climate RegulationEnhance/create emergent vegetation (e.g. mangrove, saltmarsh)

+ - +/- + + + - 0/- - + + + + +

14 Climate Regulation Shoreside power (cold ironing) 0 0 0 0 + 0 0 0 0 0 0 0 0 0

15 Climate Regulation Restrict motorcraft use + 0 +/- 0 + 0 0 0 0 0 0 0 0 +

16 Climate Regulation Fuel efficiency standards 0 0 + 0 0 0 0 0 0 0 0

17 Biotic (e.g. food) Habitat restoration/creation + - + + + - + + + + +

18 Biotic (e.g. food) Habitat protection + - +/- + + - + +/- + + +

19 Biotic (e.g. food) Installation of piers/ramps - + + 0 + + 0/- +/- - - -

20 Biotic (e.g. food) Dredging/channelization - + +/- - +/- + + + + - - - -

Cu

ltu

ral

Clim

ate

Reg

ula

tio

n

21 Biotic (e.g. food) Open diversion gates + - + + + +/- 0 0 0 + 0 +/- +/- +/-

22 Biotic (e.g. food) Stock enhancement + + +/- - + + + +/-

23 Biotic (e.g. food) Increase aquaculture development - + - + +/- - 0 - 0 0 +/- 0 -

24 Biotic (e.g. food)Non-native introductions (for the purposes of food)

- + + 0 + 0 0 0 0 + +/- 0 -

25 Biotic (e.g. food)Treatment of sewage and discharge to increase aq. food production

+ + 0 + + 0 0 0 0 0 + + +

26 Biotic (e.g. food) Fishery regulation + + + + + 0 0 0 0 + + + +

27Non-biotic (e.g. fresh water, salt, sand)

Desalination - + - - - - + - 0 0 0 - - -


Salt pond creation - - - - + 0 0 - 0 0 - -


Sand mining - + - + 0 + 0 - - -

30 Physical (energy) Provide tidal power +

31 Physical (energy) Provide cooling source +

32Transportation (shipping and ports)

Installation of piers/ramps - + +/- 0/- + + 0/- +/- - - -


Dredging/channelization (for the maintenance of shipping)

- + +/- - +/- + + + + - - - -


Allowing large container shipping +/- - - - + - - -

35 Flood ProtectionWater storage: Manage water entry into estuary (e.g. flood gates, sewage)

0 - +/- +

36 Flood Protection Dredging/channelization - + + +/- - - + + +/- - 0 -

37 Flood Protection Creating levees +/- + + - - - + +/- +/- - +/0 -

38 Flood ProtectionImplementing development regulations (buffers and zoning)

+ + + + + + - - 0 + + + + +

39 Flood ProtectionImplement managed retreat (realignment)

+

40 Flood Protection Open diversion gates 0 + + + 0 +/- - 0 + 0 +/- +/0 +/-

Pro

visi

on

ing

Sto

rm P

rote

ctio

n

41 Flood ProtectionInvasive removal (e.g. mitten crab, nutria)

+/- + + 0 - +/- + + + + + 0 + +


“Pareto-efficient” options; the frontier depicts managementoptions providing the optimal delivery of the two or moreservices, given a set cost of management (Bevacqua et al.2007; Nelson et al. 2008; Polasky et al. 2008; Lester et al.2013). Management options interior to the frontier representinferior decisions, because one or more services could beincreased at no cost to any other service by using a differentmanagement option on the frontier. Therefore, the

relationship between services (i.e., the shape of the frontier)and where options lie relative to the frontier can narrow thescope of potential management decisions and reveal which,if any, services invoke strong tradeoffs.

There are a number of reasons why management wouldbe improved by adopting more explicit and systematic as-sessments of tradeoffs among services before implementingmanagement options. For one, there may often be

Table 1 (continued)

MS # Service Management Action HS DV RC CY CM BP NBP PP TR FP SS NC CP BD

42 Flood ProtectionEstuary/wetland conservation/restoration/creation

+ +/- +/- + + + +/- +/- - + + + + +

43 Shoreline StabilityEnhance/create emergent vegetation (e.g. mangrove, saltmarsh)

+ - +/- + + + - 0/- - + + + + +

44 Shoreline Stability Enhance/create seagrass + - + + + + - +/- 0/- + + + + +

45 Shoreline Stability Enhance/create barrier islands + + + + ? + - +/- - + + + +/0 +

46 Shoreline StabilityInstall revetment/riprap/ breakwater/bulkhead

- + + +/- +/- +/- + + + + +/- - 0 -

47 Shoreline Stability Beach nourishment + + + 0 - 0 0 0 0 + + - 0 -

48 Shoreline StabilityImplement managed retreat (realignment)

+ +/- +/- + + 0 0 - +/- + + 0 - +

49 Shoreline Stability Creating/maintaining cobble beach + + + 0 - 0 0 0 0 + + 0 0 +

50 Shoreline StabilityCreating/maintaining sill/salt marsh vegetation

+ - + + + + 0 0 +/- + + + +/- +

51 Nutrient Capture & CyclingTreatment of wastewater prior to discharge

+ + + + +/- +/0 0 0 0 +/- 0/- + + +

52 Nutrient Capture & CyclingEnhance/create emergent vegetation (e.g. mangrove, saltmarsh)

+ - +/- + + + - 0/- - + + + + +

53 Nutrient Capture & CyclingRestore and enhance shellfish (filtration; e.g. oysters)

+ + + + 0 + 0/- 0 - 0 +/0 + + +/-

54 Nutrient Capture & Cycling Aerate (i.e. DO maintenance) 0 + + + - + 0 0 0 0 0 + ? +

55 Nutrient Capture & Cycling Create bioswale/retention ponds + + + + + + 0 0 0 + +/0 + + +

56 Nutrient Capture & CyclingWater disposal: direct untreated water into estuary

- +/- - ? 0 - 0 0 0 + 0/- + + -

57Removal of Contaminants & Pathogens

Treatment of wastewater prior to discharge

+ + + + +/- +/0 0 0 0 +/- 0 + + +


Treatment of stormwater prior to discharge

+ +/- + + 0 - - 0 0 +/- 0 + + +


Enhance/create emergent vegetation (e.g. mangrove, saltmarsh)

+ - +/- + + + - 0/- - + + + + +


Restore and enhance shellfish (filtration; e.g. oysters)

+ 0 + + 0 + 0/- 0 - 0 +/0 + + +/-

Sto

rm P

rote

ctio

nW

ater

Qu

alit

y

61 Removal of Contaminants & Pathogens

Create bioswale/retention ponds + + + + + + 0 0 0 + +/0 + + +

62 Removal of Contaminants & Pathogens

Water disposal: direct untreated water into estuary

- +/- - ? 0 - 0 0 0 + 0/- ? + -

63Conserving Native Biodiversity

Species protection + - +/- 0 0 +/- 0/- 0/- 0/- +/- +/- +/- +/- +


Habitat restoration/creation + - +/- + + + - - 0/- +/- + + + +


Reintroduction of natives + - +/- 0 0 +/- 0/- 0/- 0/- +/0 +/0 0 +/- +


Removal of non-native species (poison or mechanical)

+ +/- + 0/- 0/- +/- 0 + +/0 0/- 0/- - 0/- +


Creating a fishery for invasives + 0 + 0 0 + 0 0 0 +/0 0 0 +/- +


Physical barriers +/- 0 - 0 0 0 0 0 - 0 0 0 0 +/-


Treatment of ballast discharge + 0 +/0 ? 0/- +/0 0 +/0 - 0 0 0 + +


Offshore ballast exchange + 0 0 ? 0 +/0 0 +/0 - 0 0 0 + +


Hull fouling regulations + 0 0 ? + +/0 0 +/0 - 0 0 0 0 +

72 Conserve Native Biodiversity Spatial closures + - +/- + + +/- - - - +/- +/- + +/- +

Co

nse

rvin

g N

ativ

e B

iod

iver

sity

Effect of management actions across services. Signs indicate a positive (+), negative (−) or neutral (0) overall effect. Though arguments cansometimes be made for the opposite effect, the assigned value represents the preponderance of evidence. A question mark indicates that there wasnot enough evidence to assign an effect. References for the cell assignments can be found in the Electronic supplementary material. The cell colorsindicate the certainty of the directional effect: high (light grey), medium (medium gray), and low (black). Cells for which the management action fora service intersects with that same service are represented in white

MS meta-service, HS aesthetic, historical, and cultural, DV development, RC recreation, CY nutrient cycling, CM climate regulation, BP biotic provisioning,NBP non-biotic provisioning, PP physical provisioning, TR transportation, FP flood protection, SS shoreline stabilization, NC nutrient capture and cycling,CP removal of contaminants and pathogens, BD conserving native biodiversity


unintended and unexpected consequences if tradeoffs areignored; the value of services may not be fully appreciateduntil they are lost and must be compensated for with in-vestments of human capital. Second, in some cases stake-holders may perceive that tradeoffs among services will bestrong even when both services could be enhanced by takinga different, previously unexplored management approach.An explicit tradeoff analysis can reduce conflict by reveal-ing win–win solutions when only suboptimal decisions arebeing pitted against one another.

The primary obstacle in real management situations toapplying an ecosystem based management (EBM) approachvia a service tradeoff analysis, is the availability of models anddata capable of predicting service delivery. However, weassert that knowing the basic shape of the frontier can informmanagement decisions even when the details of the frontierare unknown. The frontier can be derived by using complexsimulation models, empirical data, or from a conceptual un-derstanding of the system. Even a conceptual understandingcan yield benefits over a business-as-usual approach of ignor-ing service interactions. Here, we suggest a critical first step todeveloping a more sophisticated tradeoff analysis.

We developed a management option-service matrix for bayand estuarine ecosystems as a general thought experiment thatcould be further refined for individual bays and estuaries. Thequalitative impacts of different management actions typicallytaken to promote one service are evaluated for all other ser-vices potentially provided by the system. We define servicesbroadly as things people value, which includes ecosystemservices (MEA 2005) as well as biodiversity and economicactivities. Although not conventionally recognized as an

ecosystem service, we include biodiversity as a service inour matrix since several agencies (e.g., US Fish and WildlifeService) and stakeholder groups (e.g., Audubon Society) havea directive to protect native biodiversity. We consider biodi-versity here in the loosest sense to be representative ofprotecting and maintaining native species and communities,not necessarily increasing richness or evenness of either sys-tem attribute. We also include economic activities (such asproviding for transport of goods and people, and providingarea for development) as services that estuaries can providebecause managers often have to weigh the economic, socialand political costs of managing for economic activities withtraditional ecosystem services (and biodiversity).

This matrix reveals “easy”management decisions that tendto benefit most services and “challenging” management de-cisions that may benefit one service at the expense of otherservices. This matrix can be populated using expert opinionand a review of the scientific literature. In populating thematrix, we assess general outcomes that could be applied toany estuarine system (e.g., tropical and temperate) and anylocale. This type of assessment provides a general frameworkfor a feasible first step towards considering service interac-tions when it is not yet possible to develop a sophisticatedproduction function model to simulate service outcomes.

Methods

We assembled a working group of scientists and estuarinemanagers with diverse expertise in estuarine health and eco-system services. We generated a list of services (includingeconomic activities and biodiversity) that estuaries provideand grouped these into six meta-service categories (cultural,climate regulation, provisioning, storm protection, water qual-ity, and biodiversity). We also developed lists of actions usedto manage or enhance each of the services. We consideredmanagement actions that would enhance the ecosystems’natural ability to provide the service as well as humanengineered solutions. We used expert opinion, case studies,and evidence from the literature (see Electronic supplementa-ry material (ESM)) to determine the dominant effect of amanagement action on all of the other services. We assigned+ and − values to indicate overall positive or negative effects,and a null value (0) was assigned when a management actiondid not strongly impact that service. We assigned either a +/−,+/0, or 0/− value when the direction or presence of the effectwas context dependent, and we could provide examples foreach outcome. We considered the dominant direction of theeffect, recognizing that there are exceptions to some of thesedirectional effects which could be taken into account whenapplying our approach to a specific estuary. We did not assessthe magnitude of the impact of a management action on aservice, because without formal forecasting models we lacked

Efficiency Frontier

Service 1

Ser

vice

2

Fig. 1 Efficiency frontier framework. The efficiency frontier diagramillustrates the effect of different management options on two differentservices. Open circles represent inferior or suboptimal managementoptions; neither service derives substantial benefit from the manage-ment option. The filled circles along the efficiency frontier representoptimal management options. Societal values then may further informmanagement options for service preferences. Gray circles along theefficiency frontier represent management options that place extremevalue on one service over the other; whereas, black circles representmanagement options that more evenly balance the two services


an adequate method to standardize such an assessment. Wedid estimate the certainty of the effect as either high, medium,or low based on expert opinion. In many cases, this reflectedthe number of examples available from the scientific literatureor technical reports (see ESM). However, in some cases weestimated the certainty as high when no literature was avail-able because there was not a compelling logical argument for adifferent directional effect.

We assembled our findings into a management action/servicematrix with each service listed in both the rows and columns ofthe matrix. Under each row of a service heading, we listed themanagement actions that could be used to manage (i.e., con-serve, enhance, or substitute for) that particular service. Severalmanagement actions were applicable to more than one serviceand were listed more than once in the matrix.

Management actions for each of the meta-services delin-eated below were evaluated for their benefit to multiple ser-vices by using the matrix to identify those for which themajority of the cells showed a positive impact on other ser-vices. Likewise, strong tradeoffs were identified by searchingfor management actions showing overwhelmingly negativeeffects for other services.

Cultural Services

We defined cultural services as including recreational oppor-tunities (e.g., hiking, bird watching, kayaking, and recreationalfishing), aesthetic, historical, and spiritual values, as well asproviding area for development through the filling of saltmarsh and wetland habitats (e.g., San Francisco Bay commu-nities). Management actions could be taken to enhance thehistoric, aesthetic, and spiritual cultural services bymaintaining open views characteristic of low estuarine vegeta-tion, preserving historical components of estuaries (e.g., arche-ology), protecting iconic species (e.g., flamingoes, whales, seaotters, and manatees), or implementing wetland or estuaryconservation measures. Management actions we consideredfor the enhancement of recreational opportunities includedcoastal access creation or enhancement (trails, parking lots,and roads), beach creation, boating infrastructure (piers andramps), dredging for boat channels, and stock enhancement forrecreational fishing. Finally, we considered estuaries as pro-viding the cultural service of development for airports, com-mercial business, and recreational areas as they are located incoastal zones where land values are generally high. The man-agement action of “siting and development” (Table 1), includ-ed the development of existing land as well as infilling of theestuary itself to create new areas for development.

Climate Regulation Services

Projections of future climate indicate that dramatic changescan be expected in the earth’s ecosystems (Harley et al.

2006; Hoegh-Guldberg and Bruno 2010; Chen et al.2011). Increasingly, managers are grappling with the likelyconsequences of future climate change to the systems theymanage, and seeking management options to increase theresilience of estuarine ecosystems to climatic variations.However, most of these types of management actions wereintended to ameliorate the impacts of climate change (i.e.,adaptation), rather than directly affect the provisioning ofclimate regulation services. Of course, it is possible thatfuture management actions will target climate regulatingservices. This is especially true for climate mitigationthrough carbon sequestration. The possible managementaction we considered for the enhancement of carbon seques-tration included habitat protection and habitat creation orrestoration.

Estuarine managers can implement management actionsto mitigate climate change through the reduction of green-house gas emissions. Most simply, this would involve thereduction of fossil fuel combustion in the managed areas.We have considered one such action—providing shore-sidepower (also known as cold ironing or alternative maritimepower) for ships in commercial ports—that has already beenimplemented in some areas (Hall 2010). Shore-side power isexpected to have little effect on other services; it wouldimpose some infrastructure requirements and associatedcosts on ports, but would also bring local benefits, namelylower emissions of local air pollutants and greenhouse gasesto the atmosphere (Hall 2010).

Other possible measures considered for reducing fossilfuel combustion included restrictions on personalmotorcraft use and imposing fuel efficiency standards formotorized vessels in an area. A second approach to redu-cing greenhouse gas emissions would be the conversion ofhigh-emitting habitats to low-emitting habitats. For exam-ple, freshwater marshes emit relatively large quantities ofmethane and nitrous oxide, potent greenhouse gases,whereas salt marshes have minimal emissions of thesegreenhouse gases (Bridgham et al. 2006). Although thisis a possible management action, we have not consideredthis action in the matrix because there are few opportuni-ties for this type of conversion in estuarine ecosystems as aresult of technical, ecological, and social impediments.However, conversion of coastal freshwater marshes tobrackish marshes is already underway in some areas as aresult of sea level rise (Voss et al. 2013).

Provisioning Services

Within the provisioning meta-service, we identified fourspecific estuarine services: biotic provisioning (i.e., food),non-biotic provisioning (i.e., freshwater, minerals, sand andgravel), physical provisioning (i.e., energy), and transporta-tion (i.e., creation and maintenance of port facilities for


shipping). Management actions to directly promote bioticprovisioning services included imposing fishery regulations,developing aquaculture, and introducing non-native speciesto provide food. Additionally, management actions thatindirectly support fisheries by providing access includedharbor development and channel dredging. For non-bioticprovisioning, management actions included the constructionand creation of desalination plants, salt ponds, and sandmining. Physical provisioning management actions includedproviding a water source for cooling power plants andinfrastructure for tidal power. Management actions to in-crease transportation services were focused primarily onport development, through hardscaping (including breakwa-ters and/or jetties, as well as piers and docks), dredging tomaintain navigational channels, and creating port facilitiesto transport people and goods. These operations often occurat large (i.e., tens of kilometers) scales and could havesizeable impacts to other services. Impacts from hardscapingcould include: associated coastal erosion of downstreamlocalities as a function of “sediment starvation” (Ceia et al.2010) and increased wave action (Peterson and Lowe 2009),as well as erosion (or increased sedimentation) of navigationchannels (PIANC 1997).

Storm Protection Services

Estuaries can provide protection from storms and flooding andaid in the stabilization of shorelines. Mangroves, seagrassbeds, and salt marshes can attenuate waves generated bystorms and mitigate the effects to developed shorelines andinland areas (Turner 2006; Koch et al. 2009; Engle 2011).During a storm event, salt marshes and mangroves can also actas a catchment for floodwater from rivers, storm drains, run-off, and excess effluent from sewage treatment plants; waterthat would otherwise flood surrounding areas. Conversion ofmangroves to shrimp farms and filling in salt marshes fordevelopment are major threats to the continued delivery ofstorm protection services provided by estuaries (Diana 2009).While habitat alteration is decreasing the ability of estuaries toprovide storm protection services, the demand for the serviceis expected to rise because the intensity, frequency, and sever-ity of storm events is likely to increase with climate change.

Management strategies we considered that are typical forpromoting storm protection services fell under three broadcategories: shoreline hardening, control of water flow, andrestoring or maintaining living shorelines. Shoreline hard-ening involves management strategies such as installationsof bulkheads, riprap, or groins to reduce natural erosionprocesses of shorelines. Management actions that fell undercontrolling the water flow included construction of largewater diversion structures, which can release sedimentsand nutrients to marshes from rivers, thus building protec-tive salt marsh habitat or diverting flood waters away from

major population centers to prevent flooding. Lastly, livingshorelines included management strategies such as creatingor maintaining natural habitat (mangroves, sea grass beds,and salt marsh) to reduce the effects of storm surge on thesurrounding land.

Water Quality Services

For centuries, populations living near the coast havedepended on the mixing and flushing capability of tidalexchange to maintain good water quality. Since the CleanWater Act (1972), bay and estuarine managers have under-taken extensive water quality management actions to meetthe goal of protecting the health of ecological communitiesand people. The focus of managers has begun to shift fromspecific infrastructure treating point sources and non-pointsources of pollution to an integrative approach that con-siders pollution management, resource management, andhabitat restoration to provide a better natural balance. Inmany of our estuaries, water quality management actionsare occurring side-by-side with management actions focusedon providing other ecosystem services. These joint manage-ment needs are seen by the increasing efforts of the EPA andNOAA to coordinate their chief place-based managementprograms, the EPA’s National Estuary Program and NOAA’sNational Estuarine Research Reserves System.

We broke down the water quality meta-service into twoseparate services that estuaries provide: nutrient capture andcycling and the removal of contaminants and pathogens.Management actions to enhance both services included thetreatment of wastewater prior to discharge, creating andprotecting wetland vegetation and shellfish, aerating the estu-ary, creating bioswale and retention ponds, and directinguntreated water into the estuary (as opposed to coastal waters).

Biodiversity

We defined biodiversity as protecting and maintaining nativespecies and communities, not necessarily increasing richnessor evenness of either system attribute. There are many defini-tions of biodiversity that managers use and a managementaction may have a different effect depending on the definition.For example, the response of common estuarine species to aparticular management actionmay be vastly different than thatof threatened and endangered species of concern. It is there-fore principally important when applying this matrix to anindividual site to specifically identify what aspect(s) of biodi-versity one is interested in increasing or maintaining.

Management actions aimed at protecting native bio-diversity in our matrix included habitat creation or en-hancement, habitat protection, species protection, nativespecies re-introduction, and the management of invasivespecies. Management for invasive species had two main


strategies: prevention and control. Prevention measuresconsidered included ballast water treatment and regula-tions forbidding the sale and possession of non-nativespecies. Management actions considered for establishedinvasive species included: (1) poisons (herbicides, pes-ticides), (2) physical removal of the species in question,(3) biocontrol, and (4) physical barriers to keep theinvasive species within a limited area. Regulations thatimprove water quality (e.g., regulating point and non-point sources of pollution) could also maintain or en-hance native biodiversity. We did not include waterquality management in our matrix evaluation for con-serving native biodiversity since this is not the primaryintent of these measures, although we do note theirpositive effects for native biodiversity. Indeed, increas-ingly water quality management measures are incorpo-rating biodiversity conservation as an essentialcomponent, especially for stormwater management.

Results

Expert estimates of the effect of a particular managementaction on a specific service can be found in Table 1. Afterexamining the number of positive versus negative effects of amanagement action across all services, we found that, ingeneral, management actions with a net positive effect onother services outnumber management actions with net nega-tive effects (Fig. 2). The majority of the management actionsfocused on climate regulation, storm protection, and waterquality had the most net positive effects on the other servicesconsidered here (Fig. 2a). In general, management actions thathad the fewest tradeoffs with other services were those thatenhanced or conserved natural vegetation (e.g., wetlands,mangroves, seagrass beds, and salt marsh), restored and en-hanced shellfish, regulated development (i.e., buffers andzoning), enhanced barrier islands, and treated wastewater(Fig. 2b). Management actions such as shore-side power,fishery regulations, restriction of motorcraft use, aeration,and creating a fishery for already established invasive specieshad few positive effects on other services but had a negativeeffect on no more than one other service. In contrast, manage-ment actions such as sand mining, salt pond creation, desali-nation, and allowing large container shipping to occur hadgenerally negative effects on other services by a 2:1 ratio(Fig. 2b). Below we address the main results for managementactions of each of the six meta-service categories.

Cultural Services

For historical, aesthetic, and spiritual services, the managementaction of protecting viewsheds had themost conflicts with otherservices, including other cultural services. In particular,

viewshed protection had a negative effect on developmentand other services that require the alteration of habitat such asnon-biotic provisioning (i.e., sand mining and siting of a desa-lination plant) and physical provisioning (i.e., siting of a powerplant). Management of estuaries for the purpose of develop-ment had a greater proportion of negative impacts on otherservices than did the other cultural categories. In fact, develop-ment was often at odds with other cultural services (i.e., man-agement for historic, aesthetic, and spiritual services andrecreation services). This negative impact to other servicescan largely be attributed to the conversion of saltmarsh orestuary to land suitable for development.

Among cultural services, there were management actionsthat had generally positive effects on other services thatdirectly benefit people. Parking lots, piers, trails, and coastalaccess facilitate a range of recreational activities and in-crease land values. Some cultural management actions couldalso coincide positively with a range of commercial activi-ties. For example, stock enhancement can improve recrea-tional and/or commercial fisheries and, if done correctly,restore biodiversity (Lenihan et al. 2001; Grabowski andPeterson 2007). Habitat protection can improve viewshedsand maintain biodiversity, thereby supporting ecotourism.Moreover, dredging can support recreational boating, com-mercial shipping, and fisheries (i.e., by providing access tofishing boats). Management for public access can simulta-neously increase several services provided by estuaries,including transportation, food, recreation, fishing, and adja-cent development. On the other hand, increased access cangenerally have a negative effect on biodiversity.

The effect of management for cultural services on bioticprovisioning varied by cultural service. It was generallypositive for management actions that enhanced recreationwhile negative for management actions that enhanced de-velopment. Effects on non-biotic provisioning and energywere either largely negative (e.g., management actions 1–3and 5–7) and/or neutral (e.g., management actions 8, 9, and11). Overall effects of cultural management actions onshipping/transportation/ballast discharge and water qualitywere less clear or were contradictory.

Climate Regulation Services

There were no management strategies focused on climate reg-ulation that were positive across all services. However, thenumber of negative impacts to other services across all climateregulation management actions was minimal (Fig. 2b). Amongclimate regulation management actions, shore-side powerstands out because it was neutral across all other services. Thestrongest tradeoffs involved the habitat-based management ac-tions (habitat protection and habitat creation/restoration) andarea for development or non-biotic, physical and transportationprovisioning. This conflict resulted from the requirement for


mutually exclusive use of a particular area for habitat, develop-ment or extraction of non-biotic resources. A second strongtradeoff existed for restricting the use of motorcraft. The verynature of this management measure means that motorcraft userswould not be able to boat when or where they would like (incontrast to use of non-motorizedwatercraft,whichmay benefit).This tradeoff contrasted with the imposition of fuel efficiencystandards, which would impose an initial cost but over the longterm would likely be economically beneficial to motorcraftusers.

Restricting motorcraft use negatively impacted boatingactivities, but had positive effects on non-motorized recrea-tional activities such as kayaking and snorkeling, aestheticvalues, and native biodiversity (by reducing disturbance andthe number of invasive species introduced by motorcraft).

Imposing fuel efficiency standards could have a negativeeffect on motorized boating if it increased the cost of buyingmotorcraft or restricted their availability. If motorcraft usewere reduced, the overall effects would be the same as directrestrictions on motorcraft use. However, higher fuel effi-ciency would mean lower fuel costs, so the net effect of thismanagement action might be neutral.

Provisioning Services

Overall, the provisioning management actions that had thehighest positive to negative ratios for impacts on otherservices were those implemented for biotic provisioning(Fig. 2). Even within biotic provisioning though, severalmanagement actions had strong tradeoffs with other

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Fig. 2 Net effect ofmanagement actions onservices. Management actionsfor all services plotted together(a) and separately (b). Numbersreflect associated managementactions in Table 1. Closedsymbols consider matrix cellswhere any positive or negativevalue occurred (i.e., +, +/0, +/−,−, −/0, and +/−); whereas, opensymbols excluded cells withmixed effects (i.e., +/−).Isoclines of 1:1, 1:2, and 2:1distinguish net positive effectsfrom net negative effects foreach meta-service


services. For example, tradeoffs existed between dredgingand channelization (to increase access to fish and boating)and nine of the other services (Table 1). In addition, dredg-ing and channelization could negatively impact biotic pro-visioning itself if the sedimentation from these activitiesaffects larvae or adults of species that are harvested bypeople. Increased turbidity from dredging could also harmseagrass beds, and the deposition of dredged spoil materialcould have severe benthic and fish community impacts bothinside and outside of estuaries where the material is re-leased, especially during beach renourishment (Lindemanand Snyder 1999; Bishop et al. 2006).

Research reviewed indicated that few biotic provisioningmanagement actions had no influence on other services, al-though relatively little is known about effects on servicesrelated to material cycling. Fishery regulation had the fewesttradeoffs of biotic provisioning management actions on otherservices, and included only positive and neutral effects. Stockenhancement also had mostly positive influences on otherservices (Table 1; Fig. 2). Habitat protection, restoration, andenhancement had mostly positive effects across the entirematrix (Table 1, Fig. 2), but there were also tradeoffs for someservices (i.e., development, non-biotic provisioning, physicalprovisioning, and transportation) (Table 1). Management ac-tions associated with habitat protection for the purposes ofenhancing fisheries usually had a substantial positive impacton other services.

In contrast to biotic provisioning, management actions fornon-biotic, physical and transportation services had a lowerpositive to negative services effect ratio (Fig. 2b). The man-agement actions that had the most negative effects on otherservices were desalination, salt pond creation, and sand min-ing. Desalination had negative impacts on biotic provisioningservices as well as other services through discharges of brinesand releases of toxic metals (Roberts et al. 2010), particularlyin areas with little water exchange, and has been shown toimpact soft sediment and plant communities (Roberts et al.2010). Furthermore, salt ponds have led tomajor deforestationin some coastal areas. In Mozambique, salt production rankssecond among human activities contributing to mangrovedeforestation, occurring at an estimated rate of 1,800 hayear−1

in 2001 (Semesi 1998; Barbosa et al. 2001).

Storm Protection Services

There were clearly differential, uneven, and nonlinear im-pacts of storm protection management actions on services (i.e., Lindeman and Snyder 1999; CSA 2009; Peterson andLowe 2009; Bilkovic 2011), with many management ac-tions resulting in a range of negative effects on other ser-vices (Finkl 2002; Brody et al. 2008; Peterson and Lowe2009). For example, altering intertidal shoreline with rip-rap, bulkheads, levees, and channelization in order to protect

local populations from storm surge and flooding has signif-icantly reduced nekton abundance, and size distributions ofcommon taxa in salt marsh ecosystems (reviewed inPeterson et al. 2000; Reed et al. 2006; Bilkovic andRoggero 2008). These alterations also have eliminated ormarkedly reduced intertidal habitat, which, in many bay andestuarine ecosystems, provide nursery habitat and otherservices vital to society (e.g., salt marsh, seagrass, man-grove, etc.; Finkl 2002; Peterson and Lowe 2009; Bilkovic2011). Additionally, many small-scale alterations notedabove (also including piers and docks) can have largercumulative impacts (Johnston 1994; Brody et al. 2008;Peterson and Lowe 2009) reducing biodiversity and sustain-ability of vital intertidal habitat types (Seitz et al. 2006;Bilkovic and Roggero 2008).

Although our research found no single management actiontaken to enhance or maintain storm protection had a positiveinfluence on all other services, living shoreline treatments andwetland creation scored the highest across the matrix. Forexample, building rock sills in the low marsh to stabilize marshelevations (i.e., a living shoreline approach) impacts benthicalgal production but does not influence marsh cordgrass growthin North Carolina (O’Connor et al. 2011). Finally,implementing development regulations that reduce conversionof natural habitat (such as buffers and zoning) had a positiveeffect on all but two services; non-biotic and physical provi-sioning. In this case, development regulations would likelynegatively affect the siting of a power or desalination plant.

Water Quality Services

Management actions to enhance water quality services pro-vided by estuaries generally had a positive effect on severalother services. With the exception of directing untreated waterinto an estuary, management actions to improve water qualityservices had a 2:1 or higher ratio of positive to negative effectson other services (Fig. 2). In this case, engineered systems (e.g., multi-million dollar sewage treatment or stormwater treat-ment plants) did not incur stronger tradeoffs than more naturalmanagement actions (i.e., saltmarsh and shellfish restorationand bioswales). However, a sewage treatment plant in generalwill be more effective than saltmarsh and shellfish restorationfor improving water quality.

The restoration of salt marshes and enhancement of shell-fish, particularly oysters, can increase an estuary’s ability toimprove water quality through filtration of contaminants andpathogens (Cerrato et al. 2004; Lipton 2004; Newell and Koch2004; zu Ermgassen et al. 2013), though consuming theshellfish themselves has led to norovirus outbreaks in humans(Webby et al. 2007). Moreover, the establishment, protection,and enhancement, of oyster reefs had multiple positive effectson other services. Oyster beds have increased recreationalfisheries, tourism, element cycling, flood protection, and


shoreline stabilization (Meyer et al. 1997; Lipton 2004;Newell et al. 2005; Piazza et al. 2005).

Biodiversity

Among management actions for biodiversity, those aimed atpreventing establishment of invasive species had the fewesttradeoffs whereas spatial closures and species protection hadthe most tradeoffs. In fact, most management actions forbiodiversity had strong tradeoffs with other services (Fig. 2;Table 1). Therefore, maintaining biodiversity alongside al-ternative uses requires substantial creativity to minimizetradeoffs. One common practice is to zone activities in timeand space. For instance, areas crucial for breeding birdsmight be closed to recreation, especially during the breedingseason. There may be some win–win opportunities, such asproviding observation points to areas where wildlife areprotected, conducting habitat restoration in a way that im-proves viewsheds, restoring plants that improve water qual-ity, reintroducing native fisheries species, or permittingfisheries for invasive pests. For example, a lionfish fisheryis being developed throughout the Caribbean, where thisfish is doing extensive damage to populations of nativefishes (Morris and Whitfield 2009).

Conservation of biodiversity has a strong spatial compo-nent. Benefits of preserving biodiversity can be global, whilethe impacts to other services are usually local. For this reason,regulations developed at large spatial scales (e.g., nationally)are often necessary to achieve the conservation of biodiversitylocally. Additionally, the impacts of management may betemporary. If biodiversity management requires alteringviewsheds (e.g., removal of exotic eucalyptus from the SanFrancisco Presidio National Park), there may be resistance tocontrolling invasives or restoring habitat until people becomeaccustomed to new viewsheds. Physical removal, habitat cre-ation, or poisoning of invasive species may have temporaryimpacts. However, when the benefits are long lasting, conser-vation trade-offs should be assessed over a long time horizon.

It is important to also consider that biodiversity can bemeasured in a number of ways and depending on whichmetric a manager applies, the management action effect onother services may be different. For example, spatial clo-sures that protect a threatened or endangered predator couldhave a negative effect on biotic provisioning (e.g., thesouthern sea otter and urchin fishery) but a spatial closureto protect an overfished species could have a positive effecton biotic provisioning.

Discussion

When applying the management-service matrix provided here(or refined for a specific bay or estuary), managers may lack

the more detailed service production models required to iden-tify actual tradeoff curves (e.g., Fig. 1). Given two services ofinterest, theymay not know the shape of the tradeoff curve norwhere current management falls relative to the frontier in thetradeoff space. We assert that our matrix framework providesan important and practical first step towards managing formultiple services, for bothminimizing tradeoffs andmanagingas close to the frontier as possible.

For each service, the matrix lists a number of managementactions that could be taken to enhance that service. In otherwords, if the service is plotted on the x-axis of the tradeoffspace, any of the management actions for that particularservice moves the system towards the right. However, thevarious management actions do not all have the same impacton the other services provided by the system; those manage-ment actions could have no effect, a positive effect, or anegative effect on another service (Fig. 2). If the effect ispositive on the other service, this action moves the systemcloser to the frontier regardless of where it was prior to theimplementation of the management intervention. If the effectis negative for the other service, then the net effect is morelikely to depend on the starting location in the tradeoff space.For a system already on the frontier, this may represent amovement along the frontier (enhancing one service whiledecreasing another in a way that is in theory optimal, althoughmay have negative social consequences depending on valuesfor one service over the other). If the system is interior to thefrontier, the negative impact on the other service is likely tomove the system further from the frontier. Similar logic ap-plies to management actions that are neutral to other services.Thus, even in the absence of detailed forecasting models, it isuseful for managers to identify matrix rows that are beneficialto numerous other services. Choosing as many of thesemultiservice management actions as possible will likely movemanagement of the system towards the frontier.

Although the matrix provides a sounding board for man-agers to determine how a proposed management action mightaffect other services, often the issues regarding balancingtradeoffs among services are socially and politically driven(Hughes et al. 2005; Palmer and Bernhardt 2006). Altman etal. (2011) discussed a qualitative approach to account formultiple human activities and tradeoffs with ecosystem ser-vices such that important components of an EBM strategyemerge. This approach can account for activities that havestrong negative effects on ecosystem services through cumu-lative and indirect effects (Altman et al. 2011). de Groot et al.(2010) also noted these tradeoffs in terms of land use/landcover planning but determined that nature conservation andplanning do not always require tradeoffs between nature anddevelopment and that investments in sustainable ecosystemuse are viewed as a “win–win” situation.

There are some important caveats to using the matrixframework as a step towards a more formal tradeoff


analysis. For one, the matrix does not provide informationabout the magnitude of the effect of a management action ona service. A large gain in one service may be socially andenvironmentally desirable despite a decrease in anotherservice, particularly if that decrease is relatively small com-pared with the increase in the first service. Finding commoncurrencies to assess tradeoffs can be difficult in many casesand should be the focus of further research. Second, thematrix lists commonly used management approaches; whichshould not be viewed as constraints. While in some cases,there are innovative approaches listed here (including so-called “soft” vs. “hard” shoreline protection approaches)that could reduce or eliminate existing tradeoffs, there maywell be additional approaches that should be investigated.Lastly, we think a matrix approach is most useful for iden-tifying “easy” (many positive effects across a row) and“challenging” (some negatives across all rows for manage-ment actions taken to enhance a particular service) choices.For tough choices, it may often be worth investing in morescience to be able to conduct a more quantitative tradeoffanalysis that can inform more nuanced decision making thatminimizes strong tradeoffs (White et al. 2012).

In applying this matrix to a specific estuary, site-specificinformation will be necessary especially in cases where thematrix indicated mixed directional effects (+/−). These typesof outcomes occurred in 12 % of the cells of our matrix andwould warrant further examination for a specific locale orsituation. For example, the management action of speciesprotection (management action 3 in the matrix) would havea different directional effect on recreation (and several otherservices) depending on the species being protected(Table 1). Lastly, our estimations of the directional effectof a management action on corresponding service had dif-ferent levels of associated certainty (Table 1). More invest-ment in the effect of a management action on a particularservice may also be warranted in cases where the certaintyof the effect is low (Table 1). Regardless of the limitations,using the matrix approach is an important first step to helpmanagers’ progress beyond single sector management.

Acknowledgments This work was funded by a grant from NOAA’sNational Sea Grant Office to S. Gaines and S. Lester. This work greatlybenefited from the input of the editor, the guest editor and two anon-ymous reviewers.

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